From 1956 through 1980, Shalev served in the Israel Defense Forces (IDF), eventually retiring as a Brigadier General. He commenced his military service in the infantry, first as a foot soldier and then as an officer in the Six Day War and other events.
By 1972-1974, Shalev had risen to the summit of Israel's military leadership, serving as Head of the Bureau of the then Chief of Staff, Major General David Elazar. This entailed working unceasingly at Elazar's side during the critical days preceding, during and following the Yom Kippur War. Shalev was an integral part of the high-level international military and political negotiations that followed the Yom Kippur War, including the famous Kilometer 101 accords with Egyptian General Gamassi, which eventually led to the Israel-Egypt peace treaty.
Following the conclusion of the war, Shalev chose to serve in the IDF's Education Corps, becoming Israel's Chief Education Officer. This position included command of IDF Radio, and the major task and challenge of restoring public confidence in the ability, vigor and spirit of the IDF and, in a larger sense, of Israeli society. He increased the study of the IDF's battle heritage and combat values, and promoted the leadership training of commanders. Shalev established the Education Corps' central officers training base and advanced the development of core theory and practice for cultivating Israeli military leadership.
Following his retirement from military service, Shalev assumed the position of Director of the Culture Authority in the Ministry of Education and Culture, as well as Chairman of the National Council of Culture and Art. He also served on the boards of a wide range of Israeli museums and cultural institutions. Within these capacities, Shalev was instrumental in the formulation and implementation of national policy regarding culture and the arts, and for advancing Israel's ties in these areas with other nations around the world. An example for one of his actions in this position, is that he pioneered the earmarking of public funding of cultural activities for schoolchildren. He also ensured the stability and integrity of archaeological endeavors in Israel by transforming the Antiquities Department into and national authority. Shalev help found the Sam Spiegel Film and Television School in Jerusalem.
Shalev viewed the challenge of extensive immigration to Israel from the former Soviet Union in the early 1990s as a tremendous cultural opportunity for the state. Accordingly, he set up an inter-departmental unit devoted to the absorption of immigrant artists. Its operation facilitated the founding of significant and groundbreaking cultural entities, such as the Ra'anana Orchestra and the Gesher Theatre Company.
In 1993 Avner Shalev accepted the position of Chairman of the Directorate of Yad Vashem. Five years after he took the helm of the institution, Shalev accepted on its behalf the coveted Israel Prize, for Special Service to Society and Country. In 2007, he once again received a nation's supreme honor, this time Spain's Prince of Asturias Prize for Concord (the Hispanic world's Nobel Prize equivalent), in the name of Yad Vashem. He also received the French Legion of Honor by President Sarkozy, at the Élysée Palace in Paris.
As leader of Yad Vashem, Shalev has dealt with the controversy over Pope Pius XII, and with the Museum's complicated relations with the Church. He has sought better access to Vatican archives for the period of Monsignor Pacelli's papacy.